According to his former Quebec Nordiques coach Michel Bergeron, even though Hunter was nicknamed the "Nuisance" on ice (La Petite Peste in French), he was known to be "humble" in the dressing room and a sort of "gentleman", close to all the players. He was the "perfect player", always the first to arrive at practice and ready to do all his best for the team. Thanks to his charisma, Hunter was a fan favourite in both Quebec and Washington. His leaving made Quebec very sad, and was seen as an obvious "mistake" linked to the team's future decline.[1]

Hunter served as the team captain for the Capitals. In the 1993 Patrick Division Semifinals between the Capitals and New York Islanders, Hunter had led his team with seven postseason goals, and was suspended 21 games for illegally and viciously checking and separating the shoulder of Isles star Pierre Turgeon.[2] This illegal check occurred after Turgeon had stolen an errant pass of Hunter's and subsequently scored. As Turgeon was celebrating, Hunter came up from behind and checked an unsuspecting Turgeon into the boards. This has gone down as one of the most condemned hits in NHL history and, as such, cemented his legacy as a controversial player. As a result of the incident, Hunter was suspended for the first 21 games of the 1993-94 season.

He broke the 1000 points barrier (and is the NHL record holder for requiring the most games to do so by a forward, at 1308, as well having the most penalty minutes when reaching that scoring milestone). He played in the NHL All-Star game in 1997.

Hunter finished off his career with the Colorado Avalanche, the successor to the Nordiques, and helped the team to reach the Western Conference finals, losing in seven games to the eventual cup winners Dallas Stars.

Hunter's sweater number (#32) was retired by the Capitals on March 11, 2000. During the ceremony, the Capitals presented Hunter with one of the penalty boxes from the Capital Centre (the Capitals former home arena), symbolic of his exceptional amount of time served for penalties.

Hunter became the co-owner, president and head coach of the London Knights of the Ontario Hockey League, which won the 2005 and 2016 Memorial Cup. On January 1, 2006, Hunter and his younger brother, fellow former NHLer Mark Hunter, as co-owners of the London Knights (Mark is the team's general manager), were named to the 2006 Mayor's New Year's Honours List for Sports by the City of London, Ontario. Hunter's older brother Dave Hunter is also a former NHLer. His son Dylan Hunter is an assistant coach for the London Knights and his other son Tucker also played for the London Knights before pursuing his education at the University of Western Ontario.

On November 28, 2011, Hunter resigned his position as head coach of the Knights to take the same position with the Washington Capitals, succeeding Bruce Boudreau.[3] His brother Mark then took over as Knights coach. Hunter's defense oriented system caused some conflict with star Alexander Ovechkin but it helped the struggling Capitals make the playoffs, where they upset the defending Stanley Cup champions Boston Bruins in the first round before being eliminated by the New York Rangers, both postseason series going to seven games. On May 14, 2012, Hunter announced he was not returning to coach the Capitals in the 2012-2013 season, choosing instead to return to the London Knights.[4]

Late in the deciding Game 6 of the 1993 Patrick Division Semifinals between the Capitals and New York Islanders, Pierre Turgeon stole the puck from Hunter and scored, putting the game out of reach. Hunter, who was trailing Turgeon on the play, checked Turgeon well after the goal as he started to celebrate. Turgeon sustained a separated shoulder from the hit, causing him to miss all but Game 7 against the Pittsburgh Penguins in the second round, as well as most of the series against the Montreal Canadiens in the conference finals. New NHL CommissionerGary Bettman, who had earlier promised to crack down on violence, suspended Hunter for the first 21 games of the 1993–94 season—at the time, the longest suspension in league history for an on-ice incident (in terms of games missed). Years later, Hunter admitted that he'd gone too far.[5]

With amassing a staggering 3565 penalty minutes, Hunter currently has the second-most penalty minutes in NHL history, after Dave "Tiger" Williams (although Hunter played 1,407 games to Williams' 962). When the Capitals retired his No. 32 jersey, he was presented with the penalty box from the demolished Capital Centre at the retirement ceremony. Hunter is the only NHL player ever to score over 1,000 points and rack up over 3,000 penalty minutes (1,020 points and 3,565 PIMs over 1,407 NHL games).

As of the end of the 2005–06 NHL season, he holds the record for most number of playoff games played without playing for a Stanley Cup-winning team, at 186 games. He scored in overtime for Quebec in Game 5 of their 1982 opening round best-of-five series vs. the Montreal Canadiens, and in 1988 scoring against Ron Hextall on a breakaway in overtime for Washington in Game 7 of their opening round best-of-7 series vs. the Philadelphia Flyers, making Hunter the first player in NHL history to score two overtime series-clinching goals in the playoffs.

In July 2006, Hunter was arrested and charged with DUI.[6] The charges were dropped when the presiding judge ruled that his rights under the Canadian Charter of Rights and Freedoms were violated for unlawful detention and being denied his right to his lawyer.

In September 2005, Hunter was suspended by the Ontario Hockey League for 4 games after a player left the bench to initiate a fight in an exhibition game.

On January 20, 2006, Hunter was suspended for 2 games and his team was fined $5,000 for Hunter's off ice abuse of the officials. In May 2006, Hunter was fined $5,000 by the OHL for criticizing officials after the Knights were eliminated from the playoffs in 4 straight games. In September 2006, Hunter was suspended by the OHL for 2 games after forward Matt Davis left the bench to engage in a fight during a game; OHL rules state that there is an automatic suspension for both the player and the coach if a player leaves the bench to become involved in an altercation.